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Started as a broadsheet in 1998, the Rail became a full-format publication in 2000, under the direction of publisher Phong Bui and then-editor Theodore Hamm. It was originally to be read on the L train between Manhattan and Brooklyn, but quickly expanded to its current form. Bui comments that it's largely the support of the art community and funding from art foundations that makes it possible for each section to offer their equal and indispensable voices to the journal. Hamm notes that the Rail's non-profit funding, largely provided by private donors, has preserved the magazine's original aspiration to publish a crucible of "slanted opinions, artfully delivered."[2]

The Rail, organized as a 501(c)(3)non-profit, is unusual for a periodical in that the respective editor of each section has editorial autonomy. Sections include: Field Notes (political coverage and commentary), Art (interviews with artists and art historians), Artseen (reviews of art exhibits), Art Books (reviews of art publications), Books (reviews of fiction, nonfiction, and poetry), Music (album and concert reviews), Dance (dance criticism), Film (film criticism), Theater (theater and performance criticism), Fiction (original and newly translated fiction), and Poetry (experimental poetry). Each issue, from February 2012 onwards,[3] also includes a Critics Page section directed by a guest editor that focuses on a particular critical theme or issue.[4]

The Brooklyn Rail has been endorsed by a number of prominent members of the New York art and literary community. The American painter and photographer Chuck Close called the Rail, "This generation's organ of choice in which art historians, critics, and artists themselves weigh in on the most significant art being shown as well as little known and often overlooked work by emerging, middle, and older aged artists."

Robert Storr has called it "the murmur of the city in print." Paul Auster has said that it "covers the waterfront in a highly responsible and original way, mixing controversial political journalism with poetry, the arts, and nearly everything else of importance in this complex, ever-changing city." Former Nation publisher Victor Navasky considered it "a non-establishment paper that questioned the establishment's assumptions without falling victim to the counterculture's pieties."

For the late Nancy Spero, the paper was "an eminently readable, informative, and intellectually wide-ranging publication, alert to current trends, controversies, and ideas, and filled with necessary information." John Ashbery called it "a newspaper that cares about literature and the arts and isn't afraid to say so."

The Late Henry Luce III once noted that, "Years ago the most famous newspaper in Brooklyn was the Brooklyn Eagle. The rail is also a bird, and so it is fitting that the Eagle’s successor is The Brooklyn Rail. It is a splendid publication that covers the arts, politics, and culture. I heartily recommend it.” [6]